Dendritic Spine Viscoelasticity and Soft-Glassy Nature: Balancing Dynamic Remodeling with Structural Stability

Smith, Benjamin; Roy, Hugo Le; Koninck, Paul De; Grütter, Peter; Koninck, Yves De

doi:10.1529/biophysj.106.092361

Cited by 30 publications

(29 citation statements)

References 72 publications

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“…Our data are consistent with recent atomic force microscope measurements that record five-fold greater viscosity in dendritic spines than in cell body (Smith et al 2007). (ii) Macromolecular crowding: Sieving and excluded volume effects associated with macromolecular crowding cannot presently be studied well by Smoldyn.…”

Section: In Neuronssupporting

confidence: 92%

“…The simulated "best-fit" (see Section 4) estimate was ca. 20 cp; roughly two-fold lower than viscosity reported for dendritic spines (Smith et al 2007). The FRAP curve expected if the viscosity was that measured from FRAP of animal cells (3.2 cp (Swaminathan et al 1997)) is also shown for comparison.…”

Section: Frap and Rfp Based Measurement Of Cytoplasmic Viscositymentioning

confidence: 71%

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Sequestration of CaMKII in dendritic spines in silico

et al. 2011

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Calcium calmodulin dependent kinase II (CaMKII) is sequestered in dendritic spines within seconds upon synaptic stimulation. The program Smoldyn was used to develop scenarios of single molecule CaMKII diffusion and binding in virtual dendritic spines. We first validated simulation of diffusion as a function of spine morphology. Additional cellular structures were then incorporated to simulate binding of CaMKII to the post-synaptic density (PSD); binding to cytoskeleton; or their self-aggregation. The distributions of GFP tagged native and mutant constructs in dissociated hippocampal neurons were measured to guide quantitative analysis. Intra-spine viscosity was estimated from fluorescence recovery after photo-bleach (FRAP) of red fluorescent protein. Intra-spine mobility of the GFP-CaMKIIα constructs was measured, with hundred-millisecond or better time resolution, from FRAP of distal spine tips in conjunction with fluorescence loss (FLIP) from proximal regions. Different FRAP \ FLIP profiles were predicted from our Scenarios and provided a means to differentiate binding to the PSDs from self-aggregation. The predictions were validated by experiments. Simulated fits of the Scenarios provided estimates of binding and rate constants. We utilized these values to assess the role of self-aggregation during the initial response of native CaMKII holoenzymes to stimulation. The computations revealed that self-aggregation could provide a concentration-dependent switch to amplify CaMKII sequestration and regulate its activity depending on its occupancy of the actin cytoskeleton.

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Section: In Neuronssupporting

confidence: 92%

Section: Frap and Rfp Based Measurement Of Cytoplasmic Viscositymentioning

confidence: 71%

Sequestration of CaMKII in dendritic spines in silico

et al. 2011

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“…Although the main mechanical indicator is taken to be elasticity, rheological parameters have also been extracted from living cells using various approaches [129][130][131]. Indentation approaches have been used in conjunction with scanning to produce force maps [41][42][43][44]132] or in single spots on living cells to measure time dependence [125,127].…”

Section: Introductionmentioning

confidence: 99%

An historical perspective on cell mechanics

Pelling

Horton

2007

Pflugers Arch - Eur J Physiol

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The physical properties of the protoplasm have long been of interest, and today, several intricate methods, including atomic force microscopy, have been employed in studies of cellular mechanics. However, many current concepts and experimental approaches actually have their beginnings over 300 years ago. Unfortunately, these pioneering studies have been all but forgotten. In this paper, we have reviewed some of the early literature on cellular mechanics to place modern work within an historical framework. It is clear that with current nanoscience approaches, modern experiments employing cell indentation, manipulation, particle rheology and micro-or nano-needle poking are now quantifying mechanical properties which were only qualitatively described 100 years ago. Aside from the variety of approaches our predecessors have employed to understand cellular mechanics, we feel an understanding of the past will help to propel nanoscience into the future. As nanophysiology and nanomedicine are developing, we as a community should take time to consider the early roots of these fields.

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“…The coefficient of diffusion of CaMKII was recently estimated to be 2 × 10 −14 m 2 s −1 in the spines of neurons by fluorescence recovery after photobleaching [102]. The molecular weight of aKP enzymes lies in the range of ~50–100 kDa (i.e., an order of magnitude below that of CaMKII [~630 kDa]).…”

Section: Methodsmentioning

confidence: 99%

A New Principle for Information Storage in an Enzymatic Pathway Model

2007

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Strong experimental evidence indicates that protein kinase and phosphatase (KP) cycles are critical to both the induction and maintenance of activity-dependent modifications in neurons. However, their contribution to information storage remains controversial, despite impressive modeling efforts. For instance, plasticity models based on KP cycles do not account for the maintenance of plastic modifications. Moreover, bistable KP cycle models that display memory fail to capture essential features of information storage: rapid onset, bidirectional control, graded amplitude, and finite lifetimes. Here, we show in a biophysical model that upstream activation of KP cycles, a ubiquitous mechanism, is sufficient to provide information storage with realistic induction and maintenance properties: plastic modifications are rapid, bidirectional, and graded, with finite lifetimes that are compatible with animal and human memory. The maintenance of plastic modifications relies on negligible reaction rates in basal conditions and thus depends on enzyme nonlinearity and activation properties of the activity-dependent KP cycle. Moreover, we show that information coding and memory maintenance are robust to stochastic fluctuations inherent to the molecular nature of activity-dependent KP cycle operation. This model provides a new principle for information storage where plasticity and memory emerge from a single dynamic process whose rate is controlled by neuronal activity. This principle strongly departs from the long-standing view that memory reflects stable steady states in biological systems, and offers a new perspective on memory in animals and humans.

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Dendritic Spine Viscoelasticity and Soft-Glassy Nature: Balancing Dynamic Remodeling with Structural Stability

Cited by 30 publications

References 72 publications

Sequestration of CaMKII in dendritic spines in silico

Sequestration of CaMKII in dendritic spines in silico

An historical perspective on cell mechanics

A New Principle for Information Storage in an Enzymatic Pathway Model

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